Jerry A. Coyne and H. Allen Orr. 2004. Sinauer Associates, Sunderland, Massachusetts. xiii + 545 pp. ISBN 0-87893-091-4. Cloth, $89.95. ISBN 0-87893-089-2. Paper, $54.95.—This is an important book, perhaps the most important work on the subject of speciation in decades. The species problem—explaining the origin of discrete groups living together in nature—is undoubtedly one of the greatest questions in all of biology. I found the book's logic extremely compelling. The authors first establish the existence of the phenomena under study—in this case, the reality of species. They unapologetically justify the biological species concept as an appropriate framework for studying the origin of species. And they are explicit about what they consider to be the central conceptual theme in speciation research: the origin and evolution of reproductive isolating barriers. Coyne and Orr do not dabble in semantics or philosophy, and the book cuts quickly to the process of species formation, relegating the traditional debate (or quagmire) over species concepts to a carefully worded appendix.
The remainder of the book is a tour and status review of the most significant facets of the speciation process: the geography of speciation, the nature of isolating barriers, the genetics of reproductive isolation, speciation by reinforcement, polyploidy, speciation by hybridization, the relative importance of natural selection and genetic drift, and macroevolutionary considerations. Each chapter follows a predictable format: the authors examine theoretical and experimental evidence, as well as evidence from nature. They critically revisit the literature (including their own work) and provide their own conclusions and synthesis. Through it all, the authors demand testable hypotheses and insist on examples from nature wherever possible. Such hard-nosed empiricism, from two scientists who clearly understand the theory, is very refreshing.
Some readers may find Coyne and Orr to be overly critical—perhaps downright negative—in their assessment of previous research. They hold all studies to a hard standard, and it occasionally seems difficult to do anything properly in their world. But they are at least consistent, and they clearly indicate what needs to be done in future studies. Their extensive discussion of sympatric speciation (Chapter 4) is a good example of this. To satisfy sympatric speciation, they hold a long list of potential cases to extreme scrutiny and a standard of evidence that is difficult to obtain. They conclude that, although several promising cases exist, sympatric speciation appears to receive far more attention than it warrants. One may disagree with their dismissal of some putative cases of sympatric speciation, or with their null hypothesis of allopatry—that speciation is allopatric until proven sympatric. But in the end, the lack of evidence for sympatric speciation when it should be detected (e.g. among species on small oceanic islands or among host-specific parasites) makes it difficult to believe that speciation under sympatric conditions is common.
One of the many highlights of the book is a lucid discussion of postzygotic isolation (Chapter 7). Why do hybrids often suffer reduced fitness, and what are the genetic and ecological bases of such fitness reduction? The evolution of postzygotic isolation through accumulation of genic incompatibilities is treated at length, because such gene interactions may be a critical ingredient in allopatric and parapatric speciation. Postzygotic isolation can arise because interbreeding between genetically divergent populations brings together alleles that have never been tested by natural selection in the same genome. Hybrid progeny, which may comprise a mixture of derived alleles that normally do not occur together, suffer reduced fitness because of between-locus incompatibilities. Of course, such incompatibilities may be complex, involving many loci, and there may be many such incompatibilities separating a pair of sister species, each contributing to reproductive isolation.
It now seems clear that such incompatibilities in diverging populations play a large role in the evolution of postzygotic isolation, and much of our understanding of the issue derives from the authors' own work on the relationship between genetic divergence and reproductive isolation. In Chapter 8 (Genetics of Postzygotic Isolation), they review recent work on the types of genes that cause postzygotic isolation, the developmental consequences of genic incompatibilities, the numbers of genes contributing to postzygotic isolation, and more. The authors do an excellent job with those complex issues, particularly the question of how many genes cause postzygotic reproductive isolation—a difficult question to frame, much less answer. A pair of closely related but reproductively isolated species may now be separated by hundreds of incompatibilities, but complete postzygotic isolation may have originally been caused by a small fraction of the current incompatibilities. And every case may be unique: there may be thousands of possible non-overlapping paths to complete postzygotic isolation.
The most exciting and novel aspect of the book is its extensive use of phylogenetic and comparative approaches to address the evolution of reproductive isolation. Coyne and Orr do not simply make passing reference to the implications of speciation mechanisms for macroevolutionary pattern. Rather, they claim that macroevolutionary studies themselves may hold the key to understanding mechanisms of speciation. With the recent proliferation of molecular phylogenetic data, there has been a resurgence of interest in rates of evolutionary diversification. It is now possible to ask questions like “how much do evolutionary rates vary among passerine clades” and (perhaps more interestingly) “why do evolutionary rates vary among passerine clades?” In the latter question, we are primarily interested in how individual traits within species, or properties of species themselves, relate to rates of speciation and extinction. There are now many examples of traits that are positively correlated with diversification rates (Chapter 12: Speciation and Macroevolution)—traits associated with sexual selection in animals, for example.
Coyne and Orr propose that such correlations can be used to infer the isolating barriers that typically cause speciation: if a trait creates additional isolating barriers when reproductive isolation is already complete, how can that trait increase rates of speciation? Traits that increase speciation rates should thus be primary causes of reproductive isolation. That line of reasoning helps address a fundamental problem that creeps up repeatedly throughout the book: given that many pairs of sister species are separated by multiple isolating barriers, how can we ever determine the nature of the barrier(s) that initially caused reproductive isolation? The macroevolutionary approach is not without problems, because traits showing positive correlations with diversification rates could do so by either increasing speciation rates or decreasing extinction rates. However, the authors cautiously suggest a way to distinguish among those alternatives, and they conclude that such comparative analyses may be the best method of identifying isolating barriers important in speciation.
In summary, this book deserves to be read by evolutionary biologists, ecologists, and natural historians alike. The text is eminently readable, and the authors move seamlessly between molecular and classical genetics, mathematical theory, ecology, and comparative biology to review ideas both old and new. We see how traditionally disparate research traditions complement the study of reproductive isolation. Above all, it is the authors' remarkable gift for synthesis that makes the book so valuable. With its publication, Coyne and Orr have laid the foundation for a 21st-century research program on the biology of speciation.